Effect of weight and frontal area of external telemetry packages on the kinematics,activity levels and swimming performance of small‐bodied sharks

This study sought to observe the effects of submerged weight and frontal cross‐sectional area of external telemetry packages on the kinematics, activity levels and swimming performance of small‐bodied juvenile sharks, using lemon sharks Negaprion brevirostris (60–80 cm total length, L_T) as a model species. Juveniles were observed free‐swimming in a mesocosm untagged and with small and large external accelerometer packages that increased frontal cross‐sectional area of the animals and their submerged weight. Despite adhering to widely used standards for tag mass, the presence of an external telemetry package altered swimming kinematics, activity levels and swimming performance of juvenile N. brevirostris relative to untagged individuals, suggesting that tag mass is not a suitable standalone metric of device suitability. Changes in swimming performance could not be detected from tail‐beat frequency, which suggests that tail‐beat frequency is an unsuitable standalone metric of swimming performance for small N. brevirostris. Lastly, sharks experienced treatment‐specific changes in activity level and swimming kinematics from morning to afternoon observation. Therefore, the presence of external telemetry packages altered the kinematics, activity levels and swimming performance of small young‐of‐the‐year N. brevirostris and these data may therefore be relevant to other similar‐sized juveniles of other shark species.     

Population variation in the thermal response to climate change reveals differing sensitivity in a benthic shark

Many species with broad distributions are exposed to different thermal regimes which often select for varied phenotypes. This intraspecific variation is often overlooked but may be critical in dictating the vulnerability of different populations to environmental change. We reared Port Jackson shark (Heterodontus portusjacksoni) eggs from two thermally discrete populations (i.e. Jervis Bay and Adelaide) under each location's present‐day mean temperatures, predicted end‐of‐century temperatures and under reciprocal‐cross conditions to establish intraspecific thermal sensitivity. Rearing temperatures strongly influenced ?O_2Max and critical thermal limits, regardless of population, indicative of acclimation processes. However, there were significant population‐level effects, such that Jervis Bay sharks, regardless of rearing temperature, did not exhibit differences in ?O_2Rest, but under elevated temperatures exhibited reduced maximum swimming activity with step‐wise increases in temperature. In contrast, Adelaide sharks reared under elevated temperatures doubled their ?O_2Rest, relative to their present‐day temperature counterparts; however, maximum swimming activity was not influenced. With respect to reciprocal‐cross comparisons, few differences were detected between Jervis Bay and Adelaide sharks reared under ambient Jervis Bay temperatures. Similarly, juveniles (from both populations) reared under Adelaide conditions had similar thermal limits and swimming activity (maximum volitional velocity and distance) to each other, indicative of conserved acclimation capacity. However, under Adelaide temperatures, the ?O_2Rest of Jervis Bay sharks was greater than that of Adelaide sharks. This indicates that the energetics of cooler water population (Adelaide) is likely more thermally sensitive than that of the warmer population (Jervis Bay). While unique to elasmobranchs, these data provide further support that by treating species as static, homogeneous populations, we ignore the impacts of thermal history and intraspecific variation on thermal sensitivity. With climate change, intraspecific variation will manifest as populations move, demographics change or extirpations occur, starting with the most sensitive populations.     

In situ swimming behaviors and oxygen consumption rates of juvenile lemon sharks (<Emphasis Type="Italic">Negaprion brevirostris</Emphasis>)

Knowing how often animals engage in different behaviors and their energetic costs may explain why animals behave the way they do in the wild. This study sought to investigate the relationship between the frequency of various swimming behaviors and their associated energetic costs (oxygen consumption rates) in situ for juvenile lemon sharks (Negaprion brevirostris). Behaviors were identified for captive animals and remotely observed for animals in the wild with accelerometers, and oxygen consumption rates of behaviors were estimated using acceleration-calibrated relationships. Lemon sharks rested infrequently (4.3% of deployment), and the occurrence of active swimming behaviors was inversely related to their respective oxygen consumption rates. Furthermore, time of day and tide state influenced when lemon sharks exhibited active swimming behaviors – but not resting – such that sharks were most active during the day on flooding tides. Oxygen consumption rates also differed across and within different behaviors with time of day and tide state, although mean oxygen consumption rates were highest on daytime flooding tides and uniformly reduced across all other diel and tide combinations. Despite variation in oxygen consumption rates, however, lemon shark activity occurred at 32.3–35.6% of their aerobic metabolic scope. These data do not provide a clear oxygen consumption basis for swimming behaviors observed in situ, which may have been masked by potentially stronger ecological drivers (e.g., predator-prey dynamics). However, these data are relevant to linking behavioral modifications to changes in energy use that shows much promise for addressing conservation issues in fishes.     

Using unmanned aerial vehicle (UAV) surveys and image analysis in the study of large surface‐associated marine species: a case study on reef sharks Carcharhinus melanopterus shoaling behaviour

A novel image analysis‐based technique applied to unmanned aerial vehicle (UAV) survey data is described to detect and locate individual free‐ranging sharks within aggregations. The method allows rapid collection of data and quantification of fine‐scale swimming and collective patterns of sharks. We demonstrate the usefulness of this technique in a small‐scale case study exploring the shoaling tendencies of blacktip reef sharks Carcharhinus melanopterus in a large lagoon within Moorea, French Polynesia. Using our approach, we found that C. melanopterus displayed increased alignment with shoal companions when distributed over a sandflat where they are regularly fed for ecotourism purposes as compared with when they shoaled in a deeper adjacent channel. Our case study highlights the potential of a relatively low‐cost method that combines UAV survey data and image analysis to detect differences in shoaling patterns of free‐ranging sharks in shallow habitats. This approach offers an alternative to current techniques commonly used in controlled settings that require time‐consuming post‐processing effort.     

Antagonistic effects of ocean acidification and warming on hunting sharks

Ocean warming and acidification alter the physiological performance and behaviour of many small‐bodied fishes, yet the potential interactive effects of these stressors on larger predators remains poorly understood. In particular, the combined effects of elevated temperature on metabolism and of elevated CO₂ on the behaviour of large predators may not only affect their foraging behaviour, but also the communities in which their prey live. We used a factorial design to assess how projected warming and acidification create synergies or antagonisms between physiological and behavioural processes, such as swimming activity and feeding behaviour through odour tracking and vision. Temperature increased swimming activity during feeding, independent of CO₂. Although temperature also increased motivational drive to locate and accept prey, elevated CO₂ negated chemical and visual behavioural responses that enable effective hunting. Fundamental to these effects was the negligible effect of high CO₂ in isolation, but its power to negate the positive effects of temperature when brought in conjunction. The reduced potential to locate prey due to the interactive effects of ocean acidification and warming, in combination with increases in energetic demand, suggests that energetic tradeoffs will be needed for sharks to sustain themselves at an individual and population level in a future ocean.     

Locomotion is not a privilege after birth: Ultrasound images of viviparous shark embryos swimming from one uterus to the other

Underwater ultrasound, a new tool for observing the internal body parts of aquatic animals by scuba divers, allowed us long‐term and frequent observations of the embryos of captive aquatic vertebrates. New ultrasound data of captive tawny nurse sharks (Nebrius ferrugineus) revealed that their embryos frequently migrate between the right and left uteri during gestation. This report is the first reliable evidence of active embryonic locomotion in live‐bearing vertebrates and is contradictory to the concept of “sedentary embryo” which has mainly arisen from studies of mammals. The tawny nurse shark is unique among orectolobiform sharks, in which the embryo develops by feeding on sibling eggs in utero. Thus, we hypothesized that swimming aids in an efficient search and capture of these eggs in the uterine environment.     

Reduced impact of ocean acidification on growth and swimming performance of newly hatched tropical sharks (Chiloscyllium plagiosum)

ABSTRACT

Sharks have been facing unprecedented pressure over the last decades, and ocean acidification may represent an additional threat, particularly during their most susceptible life stages. Hence, the present study aimed to investigate the effects of ocean acidification (control pCO₂ ~ 400 μatm; high pCO₂ ~ 900 μatm) on the growth, swimming performance and cholinergic system of juvenile white-spotted bamboo sharks (Chiloscyllium plagiosum). After 45 days of exposure, we observed that high CO₂ did not affect most of the end-points studied. However, somatic growth rate and the percentage of time that sharks spent swimming was significantly reduced under high CO₂ conditions. Moreover, AChE activity decreased in two of the seven brain macroareas analyzed, the telencephalon and optic lobes. As this near-threatened shark species showed small sub-lethal effects to high CO₂ levels, we argue that within a longer time-frame they can potentially reduce individual performance with cascading consequences to shark population dynamics.     

Notes on the long‐term transport of the scalloped hammerhead shark (Sphyrna lewini)

The capture and transport of scalloped hammerhead sharks (Sphyrna lewini Griffith and Smith, 1834) historically has represented a difficult, expensive, and uncertain undertaking for the public aquarium community. In this study, techniques were developed to improve the successful long‐term transport of S. lewini by mitigating some of the deleterious effects associated with hyperactivity and impaired swimming patterns. The relationship between the transport vessel size and shark sizes, numbers, and swimming behavior was considered when formulating the transport regime. By balancing these factors and adopting a comprehensive water treatment method, it was possible to extend the duration of a successful transport by up to 60 hr. Implications for the future transport of S. lewini and other free‐swimming sharks are discussed. Zoo Biol 21:243–251, 2002. © 2002 Wiley‐Liss, Inc.     

Swimming efficiency and the influence of morphology on swimming costs in fishes

Swimming performance is considered a main character determining survival in many aquatic animals. Body morphology highly influences the energetic costs and efficiency of swimming and sets general limits on a species capacity to use habitats and foods. For two cyprinid fishes with different morphological characteristics, carp (Cyprinus carpio L.) and roach (Rutilus rutilus (L.)), optimum swimming speeds (U _mc) as well as total and net costs of transport (COT, NCOT) were determined to evaluate differences in their swimming efficiency. Costs of transport and optimum speeds proved to be allometric functions of fish mass. NCOT was higher but U _mc was lower in carp, indicating a lower swimming efficiency compared to roach. The differences in swimming costs are attributed to the different ecological demands of the species and could partly be explained by their morphological characteristics. Body fineness ratios were used to quantify the influence of body shape on activity costs. This factor proved to be significantly different between the species, indicating a better streamlining in roach with values closer to the optimum body form for efficient swimming. Net swimming costs were directly related to fish morphology.     

Salinity selection and preference of the grey snapper Lutjanus griseus: field and laboratory observations

Field observations were supplemented with laboratory experiments to reveal patterns of salinity selection and preference for grey snapper Lutjanus griseus (c. 21 cm total length, L_T), an ecologically and economically important species in the south‐eastern U.S.A. Fish abundance data were examined from a long‐term field survey conducted in the mangrove habitats of Biscayne Bay, Florida, where salinities ranged from <1 to 40. First, regression analyses indicated significant, positive linear relationships with salinity for both L. griseus frequency of occurrence and concentration (density when present). These patterns are inconsistent with physiological expectations of minimizing energetic osmoregulatory costs. Next, the salinity preference and swimming activity of 11 L. griseus (ranging from 18 to 23 cm L_T) were investigated using a newly developed electronic shuttlebox system. In the laboratory, fish preferred intermediate salinities in the range of 9–23. Swimming activity (measured in terms of spontaneous swimming speed) followed a parabolic relationship with salinity, with reduced activity at salinity extremes perhaps reflecting compensation for higher osmoregulatory costs. It is suspected that the basis of the discrepancy between laboratory and field observations for size classes at or near maturity ultimately relates to the reproductive imperative to move towards offshore (high‐salinity) coral‐reef habitats, a necessity that probably overrides the strategy of minimizing osmoregulatory energetic costs.     

Blacktip reef sharks,Carcharhinus melanopterus,have high genetic structure and varying demographic histories in their Indo‐Pacific range

For free‐swimming marine species like sharks, only population genetics and demographic history analyses can be used to assess population health/status as baseline population numbers are usually unknown. We investigated the population genetics of blacktip reef sharks, Carcharhinus melanopterus; one of the most abundant reef‐associated sharks and the apex predator of many shallow water reefs of the Indian and Pacific Oceans. Our sampling includes 4 widely separated locations in the Indo‐Pacific and 11 islands in French Polynesia with different levels of coastal development. Four‐teen microsatellite loci were analysed for samples from all locations and two mitochondrial DNA fragments, the control region and cytochrome b, were examined for 10 locations. For microsatellites, genetic diversity is higher for the locations in the large open systems of the Red Sea and Australia than for the fragmented habitat of the smaller islands of French Polynesia. Strong significant structure was found for distant locations with F_ST values as high as ~0.3, and a smaller but still significant structure is found within French Polynesia. Both mitochondrial genes show only a few mutations across the sequences with a dominant shared haplotype in French Polynesia and New Caledonia suggesting a common lineage different to that of East Australia. Demographic history analyses indicate population expansions in the Red Sea and Australia that may coincide with sea level changes after climatic events. Expansions and flat signals are indicated for French Polynesia as well as a significant recent bottleneck for Moorea, the most human‐impacted lagoon of the locations in French Polynesia.     

The effect of substratum type on aspects of swimming performance and behaviour in shortnose sturgeon Acipenser brevirostrum

The swimming performance and associated swimming behaviour (i.e. substratum‐skimming, station‐holding and free swimming) were assessed in shortnose sturgeon Acipenser brevirostrum during critical swimming and endurance swimming tests over a rough and a smooth substratum. It was hypothesized that the addition of a rough substratum in the swimming flume may provide a surface for the A. brevirostrum to grip and offer an energetic advantage. Substratum type did not affect the critical swimming performance, but A. brevirostrum consistently performed more bottom behaviours (i.e. substratum‐skimming and station‐holding) while on a smooth substratum. Acipenser brevirostrum had little contact with the rough substratum until the velocity was >1 body length s^?1. Endurance swimming time was significantly lower for A. brevirostrum over the rough bottom at the highest velocity (30 cm s^?1) which may be attributed to the observed increase in free swimming and decrease in bottom behaviours. During endurance swimming, the rough substratum was mainly used at intermediate velocities, suggesting that there may be a stability cost associated with being in contact with the rough substratum at certain velocities.     

Combining abundance and performance data reveals how temperature regulates coastal occurrences and activity of a roaming apex predator

The redistribution of species has emerged as one of the most pervasive impacts of anthropogenic climate warming, and presents many societal challenges. Understanding how temperature regulates species distributions is particularly important for mobile marine fauna such as sharks given their seemingly rapid responses to warming, and the socio‐political implications of human encounters with some dangerous species. The predictability of species distributions can potentially be improved by accounting for temperature's influence on performance, an elusive relationship for most large animals. We combined multi‐decadal catch data and bio‐logging to show that coastal abundance and swimming performance of tiger sharks Galeocerdo cuvier are both highest at ~22°C, suggesting thermal constraints on performance may regulate this species' distribution. Tiger sharks are responsible for a large proportion of shark bites on humans, and a focus of controversial control measures in several countries. The combination of distribution and performance data moves towards a mechanistic understanding of tiger shark's thermal niche, and delivers a simple yet powerful indicator for predicting the location and timing of their occurrences throughout coastlines. For example, tiger sharks are mostly caught at Australia's popular New South Wales beaches (i.e. near Sydney) in the warmest months, but our data suggest similar abundances will occur in winter and summer if annual sea surface temperatures increase by a further 1–2°C.     

Divergence in physiological factors affecting swimming performance between anadromous and resident populations of brook charr Salvelinus fontinalis

In this study, an anadromous strain (L) and a freshwater‐resident (R) strain of brook charr Salvelinus fontinalis as well as their reciprocal hybrids, were reared in a common environment and submitted to swimming tests combined with salinity challenges. The critical swimming speeds (U_crit) of the different crosses were measured in both fresh (FW) and salt water (SW) and the variations in several physiological traits (osmotic, energetic and metabolic capacities) that are predicted to influence swimming performance were documented. Anadromous and resident fish reached the same U_crit in both FW and SW, with U_crit being 14% lower in SW compared with FW. The strains, however, seemed to use different underlying strategies: the anadromous strain relied on its streamlined body shape and higher osmoregulatory capacity, while the resident strain had greater citrate synthase (FW) and lactate dehydrogenase (FW, SW) capacity and either greater initial stores or more efficient use of liver (FW, SW) and muscle (FW) glycogen during exercise. Compared with R_♀L_♂ hybrids, L_♀R_♂ hybrids had a 20% lower swimming speed, which was associated with a 24% smaller cardio‐somatic index and higher physiological costs. Thus swimming performance depends on cross direction (i.e. which parental line was used as dam or sire). The study thus suggests that divergent physiological factors between anadromous and resident S. fontinalis may result in similar swimming capacities that are adapted to their respective lifestyles.     

Effects of passive integrated transponder tagging on cortisol release,aerobic metabolism and growth of the Gulf killifish Fundulus grandis

The effects of passive integrated transponder (PIT) tagging on cortisol release, standard metabolic rate (SMR) and daily specific growth rate (G_S) were evaluated in the Gulf killifish, Fundulus grandis, a small estuarine fish native to the Gulf of Mexico. Cortisol release by individual fish was measured non-invasively prior to PIT tagging, immediately after tagging and once per week for 1 month following tagging. Within the first 2 h of tagging, cortisol release rates were significantly elevated compared with values measured prior to tagging and significantly higher than that of fish handled identically except not implanted with PIT tags. By 1 week after PIT tagging, cortisol release rates returned to control levels. SMR, determined by intermittent-flow respirometry and G_S, defined as per cent change in body mass per day, were measured prior to PIT tagging and weekly for 1 month after tagging. Neither SMR nor G_S was significantly different in tagged v. untagged fish for the duration of the study. One month after tagging, haematocrit, plasma cortisol, blood glucose and blood lactate did not differ between tagged and untagged individuals. Therefore, after a transient stress response that subsides within 1 week, PIT tagging had no significant effects on these physiological variables in F. grandis, validating its use as a method of marking this and other small fishes.     

Heart rates of Atlantic salmon Salmo salar during a critical swim speed test and subsequent recovery

In this study, heart rate (HR) bio-loggers were implanted in the abdominal cavity of 12 post-smolt Atlantic salmon Salmo salar weighing 1024 ± 31 g and acclimated to 12°C sea water. One week after the surgical procedure, a critical swim speed (U_crit) test was performed on tagged and untagged conspecifics, whereafter tagged fish were maintained in their holding tanks for another week. The U_crit was statistically similar between tagged and untagged fish (2.67 ± 0.04 and 2.74 ± 0.05 body lengths s⁻¹, respectively) showing that the bio-logger did not compromise the swimming performance. In the pre-swim week, a diurnal cycle was apparent with HR peaking at 65 beats min⁻¹ during the day and approaching 40 beats min⁻¹ at night. In the U_crit test, HR increased approximately exponentially with swimming speed until a plateau was reached at the final speed before fatigue with a maximum of 85.2 ± 0.7 beats min⁻¹. During subsequent recovery tagged fish could be divided into a surviving group (N = 8) and a moribund group (N = 4). In surviving fish HR had fully recovered to pre-swim levels after 24 h, including reestablishment of a diurnal HR cycle. In moribund fish HR never recovered and remained elevated at c. 80 beats min⁻¹ for 4 days, whereafter they started dying. We did not identify a proximal cause of death in moribund fish, but possible explanations are discussed. Tail beat frequency (TBF) was also measured and showed a more consistent response to increased swimming speeds. As such, when exploring correlations between HR, TBF and metabolic rates at different swimming speeds, TBF provides better predictions. On the contrary, HR measurements in free swimming fish over extended periods of time are useful for other purposes such as assessing the accumulative burden of various stressors and recovery trajectories from exhaustive exercise.     

Odor tracking in sharks is reduced under future ocean acidification conditions

Recent studies show that ocean acidification impairs sensory functions and alters the behavior of teleost fishes. If sharks and other elasmobranchs are similarly affected, this could have significant consequences for marine ecosystems globally. Here, we show that projected future CO₂ levels impair odor tracking behavior of the smooth dogfish (Mustelus canis). Adult M. canis were held for 5 days in a current‐day control (405 ± 26 μatm) and mid (741 ± 22 μatm) or high CO₂ (1064 ± 17 μatm) treatments consistent with the projections for the year 2100 on a ‘business as usual’ scenario. Both control and mid CO₂‐treated individuals maintained normal odor tracking behavior, whereas high CO₂‐treated sharks significantly avoided the odor cues indicative of food. Control sharks spent >60% of their time in the water stream containing the food stimulus, but this value fell below 15% in high CO₂‐treated sharks. In addition, sharks treated under mid and high CO₂ conditions reduced attack behavior compared to the control individuals. Our findings show that shark feeding could be affected by changes in seawater chemistry projected for the end of this century. Understanding the effects of ocean acidification on critical behaviors, such as prey tracking in large predators, can help determine the potential impacts of future ocean acidification on ecosystem function.     

Sexually dimorphic morphology and swimming performance relationships in wild‐type zebrafish Danio rerio

This study compared prolonged swimming performance (U_crit) between male and female Danio rerio, and characterized how body shape was associated with this performance measure in each sex. When swimming in small (n = 6) mixed‐sex groups at 28° C, males swam, on average, over 10 cm s^?1 faster than females despite being significantly smaller. Body shape was sexually dimorphic, with males and females exhibiting small, but statistically significant differences in most aspects of body shape. Body shape explained 18 and 43% of the variation in U_crit among males and females. In general, effects of body shape on swimming performance appeared to be sex limited, whereby different aspects of body shape affected performance in each sex, although the contribution of the distance between pelvic and anal fins to swimming performance was weakly sexually antagonistic.     

Is post‐feeding thermotaxis advantageous in elasmobranch fishes?

The effects of post‐feeding thermotaxis on ileum evacuation and absorption rates were examined in the laboratory using two elasmobranch species, the Atlantic stingray Dasyatis sabina, which inhabits thermally variable environments, and the whitespotted bamboo shark Chiloscyllium plagiosum, a stenothermic fish living on Indo‐Pacific reefs. Experiments at temperatures similar to those experienced in nature revealed temperature change had no significant effect on C. plagiosum absorption or evacuation rates, suggesting stenothermic sharks cannot exploit temperature differences as a means to improve digestion efficiency. On the other hand, D. sabina showed significantly lower evacuation and absorption rates at lower temperatures. The relative decrease was greater for evacuation (Q₁₀ = 3·08) than absorption rates (Q₁₀ = 2·20), resulting in a significant increase in total absorption, suggesting D. sabina can benefit from using shuttling behaviour to exploit thermal variability in their environment to maximize energetic uptake.     

Laboratory protocol to calibrate sea lamprey (<Emphasis Type="Italic">Petromyzon marinus</Emphasis> L.) EMG signal output with swimming

A correct application of electromyogram (EMG) telemetry in the field can be a powerful tool to evaluate activity patterns and swimming strategies of fishes. We evaluated the swim performance of seven untagged sea lampreys (Petromyzon marinus L.) with critical swim speed (U _crit) tests. The average U _crit observed was c. 1.03 ms⁻¹ (i.e., 1.14 BL s⁻¹). The strongest reotaxic response was observed during tests using water velocities between 0.4 ms⁻¹ and 0.8 ms⁻¹. During two consecutive years (i.e., 2004 and 2005), in order to model upstream migration of sea lampreys with CEMG transmitters (Lotek Wireless), we calibrated EMG signal with swim speed. A high correlation between EMG records and swim speed was observed in both years (r ² = 0.74–0.93). However, in spite of methodology improvements and standardization in the second year of study, differences in intercepts and slopes were observed between individuals, making the determination of a unique calibration equation for all tagged animals unfeasible. Therefore, it appears to be necessary to obtain the relationship between EMG signals and swimming speed for each lamprey using laboratory procedures, prior to release in the wild. It is unknown whether this variability results from individual locomotor behaviour, physiological state and/or variation in placement and functioning of the EMG transmitters. The results of five laboratory calibrated lampreys, released in the River Mondego, revealed considerable differences between swim speeds calculated with EMG signal (calibration equation) and ground speed therefore it was not possible to successfully calibrate the EMG signal output with swimming speed. In order to accomplish this, longer continuous swimming tests in laboratory are necessary. Nevertheless, the calibrated swimming effort gives reliable information about the swimming behaviour and permits comparison of the results between animals.